Tools for connectomic reconstruction and analysis of a female<i>Drosophila</i>ventral nerve cord

Azevedo, Anthony W.; Lesser, Ellen; Mark, Brandon; Phelps, Jasper S.; Elabbady, Leila; Kuroda, Sumiya; Sustar, Anne; Moussa, Anthony J.; Khandelwal, Avinash; Dallmann, Chris J.; Agrawal, Sweta; Lee, Su-Yee J.; Pratt, Brandon; Cook, Andrew W.; Skutt-Kakari, Kyobi; Gerhard, Stephan; Lu, Ran; Kemnitz, Nico; Lee, Ki-Suk; Halageri, Akhilesh; Castro, Manuel; Ih, Dodam; Gager, Jay; Tammam, Marwan; Dorkenwald, Sven; Collman, Forrest; Schneider-Mizell, Casey M; Brittain, Derrick; Jordan, Chris; Dickinson, Michael H.; Pacureanu, Alexandra; Seung, H. Sebastian; Macrina, Thomas; Lee, Wei-Chung Allen; Tuthill, John C.

doi:10.1101/2022.12.15.520299

Cited by 36 publications

(104 citation statements)

References 136 publications

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“…To better understand the logic of these connections, we focused on the region of the ventral nerve cord that controls the front legs — the T1 neuromere — because T1 motor neurons have been mapped to their muscle targets and actions on the leg joints 67 . In T1, we identified all the monosynaptic and disynaptic outputs of DNa02 and DNg13, and we determined the likely neurotransmitter for each disynaptic connection by identifying the hemilineage of the interposed cell, as neurons within the same hemilineage generally release the same neurotransmitter 68, 69 .…”

Section: Resultsmentioning

confidence: 99%

Fine-grained descending control of steering in walkingDrosophila

Yang,

Brezovec,

Serratosa Capdevila

et al. 2023

Preprint

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Locomotion involves rhythmic limb movement patterns that originate in circuits outside the brain. Purposeful locomotion requires descending commands from the brain, but we do not understand how these commands are structured. Here we investigate this issue, focusing on the control of steering in walking Drosophila. First, we describe different limb "gestures" associated with different steering maneuvers. Next, we identify a set of descending neurons whose activity predicts steering. Focusing on two descending cell types downstream from distinct brain networks, we show that they evoke specific limb gestures: one lengthens strides on the outside of a turn, while the other attenuates strides on the inside of a turn. Notably, a single descending neuron can have opposite effects during different locomotor rhythm phases, and we identify networks positioned to implement this phase-specific gating. Together, our results show how purposeful locomotion emerges from brain cells that drive specific, coordinated modulations of low-level patterns.

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Section: Resultsmentioning

confidence: 99%

Fine-grained descending control of steering in walkingDrosophila

Yang,

Brezovec,

Serratosa Capdevila

et al. 2023

Preprint

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“…To determine whether proprioceptor axons receive presynaptic input, we first reconstructed FeCO axons in an electron microscopy volume of a female Drosophila VNC (FANC;. We took advantage of automated tools for neuron segmentation and synapse prediction (Azevedo et al 2022), and then manually proofread each axon for accuracy. We reconstructed 19 of ~30 claw axons and 22 of ~56 hook axons in the neuromere of the left front leg (Figure 1C and S1; Video S1).…”

Section: Proprioceptor Axons From the Drosophila Leg Are Anatomically...mentioning

confidence: 99%

Presynaptic inhibition selectively suppresses leg proprioception in behavingDrosophila

Dallmann,

Luo,

Agrawal

et al. 2023

Preprint

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The sense of proprioception is mediated by internal mechanosensory neurons that detect joint position and movement. To support a diverse range of functions, from stabilizing posture to coordinating movements, proprioceptive feedback to limb motor control circuits must be tuned in a context-dependent manner. How proprioceptive feedback signals are tuned to match behavioral demands remains poorly understood. Using calcium imaging in behavingDrosophila, we find that the axons of position-encoding leg proprioceptors are active across behaviors, whereas the axons of movement-encoding leg proprioceptors are suppressed during walking and grooming. Using connectomics, we identify a specific class of interneurons that provide GABAergic presynaptic inhibition to the axons of movement-encoding proprioceptors. These interneurons are active during self-generated but not passive leg movements and receive input from descending neurons, suggesting they are driven by predictions of leg movement originating in the brain. Predictively suppressing expected proprioceptive feedback provides a mechanism to attenuate reflexes that would otherwise interfere with voluntary movement.

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“…These results, together with the recently published draft VNC connectome (Azevedo et al, 2022), prompted us to analyze the direct wing steering muscles for innervation by MNs with both aPKC and FoxP expression. Each direct steering muscle is innervated by one single identified MN (Trimarchi and Schneiderman, 1994).…”

Section: Resultsmentioning

confidence: 95%

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning inDrosophila

Ehweiner

Brembs

2022

Preprint

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Motor learning is not only a key invention of the many new animals evolving new body plans during the Cambrian, it is also central to human existence such as in learning to speak or walk, rehabilitation after injury, or sports. Evidence suggests that all forms of motor learning may share an evolutionary conserved molecular plasticity pathway. Here we present novel insights into the molecular processes underlying a kind of motor learning in the fruit fly Drosophila, operant self-learning. We have discovered that the Forkhead Box gene FoxP is not required in the fly brain for this type of learning. Instead, atypical protein kinase C (aPKC) appears to be a central component in a plasticity process that takes place in FoxP-expressing motor neurons in the ventral nerve cord. Using CRISPR/Cas9 to knock out canonical aPKC interaction partners bazooka and the kidney and brain gene (KIBRA) in adult animals, we found that aPKC likely acts via non-canonical pathways in this form of learning. We also found that 14 but not 7 days after CRISPR/Cas9-mediated knockout of FoxP in adult animals, learning is impaired, suggesting that adult FoxP expression is required for operant self-learning.

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Tools for connectomic reconstruction and analysis of a femaleDrosophilaventral nerve cord

Cited by 36 publications

References 136 publications

Fine-grained descending control of steering in walkingDrosophila

Fine-grained descending control of steering in walkingDrosophila

Presynaptic inhibition selectively suppresses leg proprioception in behavingDrosophila

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning inDrosophila

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